Myeloid-Epithelial-Reproductive Receptor Tyrosine Kinase and Milk Fat Globule Epidermal Growth Factor 8 Coordinately Improve Remodeling after Myocardial Infarction via Local Delivery of Vascular Endothelial Growth Factor

Circulation

Volumn 133, Issue 9, 2016, Pages 826-839

  Howangyin, Kiave Yune ^a   Zlatanova, Ivana ^a   Pinto, Cristina ^a   Ngkelo, Anta ^a   Cochain, Clement ^b   Rouanet, Marie ^a   Vilar, Jose ^a   Lemitre, Mathilde ^a   Stockmann, Christian ^a   Fleischmann, Bernd K ^c   Mallat, Ziad ^a,d   Silvestre, Jean Sebastien ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Inflammation; macrophages; myocardial infarction; myocarditis; neovascularization, physiologic

Indexed keywords

LACTADHERIN; MYELOID EPITHELIAL REPRODUCTIVE RECEPTOR TYROSINE KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN; MEMBRANE ANTIGEN; MERTK PROTEIN, MOUSE; MFGE8 PROTEIN, MOUSE; MILK PROTEIN; ONCOPROTEIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE TARGETING; HEART FUNCTION; HEART INFARCTION SIZE; HEART VENTRICLE REMODELING; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; HEART INFARCTION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; SECRETION (PROCESS); TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, SURFACE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MILK PROTEINS; MYOCARDIAL INFARCTION; PHAGOCYTOSIS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR REMODELING;

EID: 84959544981     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.115.020857     Document Type: Article

References (41)

1. Szondy Z, Garabuczi E, Joós G, Tsay GJ, Sarang Z. Impaired clearance of apoptotic cells in chronic inflammatory diseases: therapeutic implications. Front Immunol. 2014;5:354. doi: 10.3389/fimmu.2014.00354.
2. Foo RS, Mani K, Kitsis RN. Death begets failure in the heart. J Clin Invest. 2005;115:565-571. doi: 10.1172/JCI24569.
3. Whelan RS, Kaplinskiy V, Kitsis RN. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol. 2010;72:19-44. doi: 10.1146/annurev.physiol.010908.163111.
4. Chen J, Carey K, Godowski PJ. Identification of Gas6 as a ligand for Mer, a neural cell adhesion molecule related receptor tyrosine kinase implicated in cellular transformation. Oncogene. 1997;14:2033-2039. doi: 10.1038/sj.onc.1201039.
5. Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R, Cohen PL, Earp HS, Matsushima GK. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature. 2001;411:207-211. doi: 10.1038/35075603.
6. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature. 2002;417:182-187. doi: 10.1038/417182a.
7. Ensslin MA, Shur BD. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding. Cell. 2003;114:405-417.
8. Silvestre JS, Théry C, Hamard G, Boddaert J, Aguilar B, Delcayre A, Houbron C, Tamarat R, Blanc-Brude O, Heeneman S, Clergue M, Duriez M, Merval R, Lévy B, Tedgui A, Amigorena S, Mallat Z. Lactadherin promotes VEGF-dependent neovascularization. Nat Med. 2005;11:499-506. doi: 10.1038/nm1233.
9. Ait-Oufella H, Kinugawa K, Zoll J, Simon T, Boddaert J, Heeneman S, Blanc-Brude O, Barateau V, Potteaux S, Merval R, Esposito B, Teissier E, Daemen MJ, Lesèche G, Boulanger C, Tedgui A, Mallat Z. Lactadherin deficiency leads to apoptotic cell accumulation and accelerated atherosclerosis in mice. Circulation. 2007;115:2168-2177. doi: 10.1161/CIRCULATIONAHA.106.662080.
10. Deroide N, Li X, Lerouet D, Van Vré E, Baker L, Harrison J, Poittevin M, Masters L, Nih L, Margaill I, Iwakura Y, Ryffel B, Pocard M, Tedgui A, Kubis N, Mallat Z. MFGE8 inhibits inflammasome-induced IL-1 production and limits postischemic cerebral injury. J Clin Invest. 2013;123:1176-1181. doi: 10.1172/JCI65167.
11. Hanayama R, Tanaka M, Miyasaka K, Aozasa K, Koike M, Uchiyama Y, Nagata S. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science. 2004;304:1147-1150. doi: 10.1126/science.1094359.
12. Kranich J, Krautler NJ, Falsig J, Ballmer B, Li S, Hutter G, Schwarz P, Moos R, Julius C, Miele G, Aguzzi A. Engulfment of cerebral apoptotic bodies controls the course of prion disease in a mouse strain-dependent manner. J Exp Med. 2010;207:2271-2281. doi: 10.1084/jem.20092401.
13. Nandrot EF, Anand M, Almeida D, Atabai K, Sheppard D, Finnemann SC. Essential role for MFG-E8 as ligand for alphavbeta5 integrin in diurnal retinal phagocytosis. Proc Natl Acad Sci USA. 2007;104:12005-12010. doi: 10.1073/pnas.0704756104.
14. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037-3047. doi: 10.1084/jem.20070885.
15. Nahrendorf M, Swirski FK. Monocyte and macrophage heterogeneity in the heart. Circ Res. 2013;112:1624-1633. doi: 10.1161/CIRCRESAHA.113.300890.
16. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122:787-795. doi: 10.1172/JCI59643.
17. Lavine KJ, Epelman S, Uchida K, Weber KJ, Nichols CG, Schilling JD, Ornitz DM, Randolph GJ, Mann DL. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. Proc Natl Acad Sci USA. 2014;111:16029-16034. doi: 10.1073/pnas.1406508111.
18. Epelman S, Lavine KJ, Beaudin AE, Sojka DK, Carrero JA, Calderon B, Brija T, Gautier EL, Ivanov S, Satpathy AT, Schilling JD, Schwendener R, Sergin I, Razani B, Forsberg EC, Yokoyama WM, Unanue ER, Colonna M, Randolph GJ, Mann DL. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity. 2014;40:91-104. doi: 10.1016/j. immuni.2013.11.019.
19. Epelman S, Lavine KJ, Randolph GJ. Origin and functions of tissue macrophages. Immunity. 2014;41:21-35. doi: 10.1016/j.immuni.2014.06.013.
20. Heidt T, Courties G, Dutta P, Sager HB, Sebas M, Iwamoto Y, Sun Y, Da Silva N, Panizzi P, van der Laan AM, van der Lahn AM, Swirski FK, Weissleder R, Nahrendorf M. Differential contribution of monocytes to heart macrophages in steady-state and after myocardial infarction. Circ Res. 2014;115:284-295. doi: 10.1161/CIRCRESAHA.115.303567.
21. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest. 1998;101:890-898. doi: 10.1172/JCI1112.
22. Stanford JC, Young C, Hicks D, Owens P, Williams A, Vaught DB, Morrison MM, Lim J, Williams M, Brantley-Sieders DM, Balko JM, Tonetti D, Earp HS 3rd, Cook RS. Efferocytosis produces a prometastatic landscape during postpartum mammary gland involution. J Clin Invest. 2014;124:4737-4752. doi: 10.1172/JCI76375.
23. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R, Offenstadt G, Lesèche G, Cohen PL, Tedgui A, Mallat Z. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:1429-1431. doi: 10.1161/ATVBAHA.108.169078.
24. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, Greenberg JI, Cheresh DA, Johnson RS. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature. 2008;456:814-818. doi: 10.1038/nature07445.
25. Fleischmann M, Bloch W, Kolossov E, Andressen C, Müller M, Brem G, Hescheler J, Addicks K, Fleischmann BK. Cardiac specific expression of the green fluorescent protein during early murine embryonic development. FEBS Lett. 1998;440:370-376.
26. Cochain C, Auvynet C, Poupel L, Vilar J, Dumeau E, Richart A, Récalde A, Zouggari Y, Yin KY, Bruneval P, Renault G, Marchiol C, Bonnin P, Lévy B, Bonecchi R, Locati M, Combadière C, Silvestre JS. The chemokine decoy receptor D6 prevents excessive inflammation and adverse ventricular remodeling after myocardial infarction. Arterioscler Thromb Vasc Biol. 2012;32:2206-2213. doi: 10.1161/ATVBAHA.112.254409.
27. Zouggari Y, Ait-Oufella H, Bonnin P, Simon T, Sage AP, Guérin C, Vilar J, Caligiuri G, Tsiantoulas D, Laurans L, Dumeau E, Kotti S, Bruneval P, Charo IF, Binder CJ, Danchin N, Tedgui A, Tedder TF, Silvestre JS, Mallat Z. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med. 2013;19:1273-1280. doi: 10.1038/nm.3284.
28. Dewald O, Zymek P, Winkelmann K, Koerting A, Ren G, Abou-Khamis T, Michael LH, Rollins BJ, Entman ML, Frangogiannis NG. CCL2/monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res. 2005;96:881-889. doi: 10.1161/01.RES.0000163017.13772.3a.
29. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science. 2010;327:656-661. doi: 10.1126/science.1178331.
30. Carlin LM, Stamatiades EG, Auffray C, Hanna RN, Glover L, Vizcay-Barrena G, Hedrick CC, Cook HT, Diebold S, Geissmann F. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell. 2013;153:362-375. doi: 10.1016/j.cell.2013.03.010.
31. Hilgendorf I, Gerhardt LM, Tan TC, Winter C, Holderried TA, Chousterman BG, Iwamoto Y, Liao R, Zirlik A, Scherer-Crosbie M, Hedrick CC, Libby P, Nahrendorf M, Weissleder R, Swirski FK. Ly-6Chigh monocytes depend on Nr4a1 to balance both inflammatory and reparative phases in the infarcted myocardium. Circ Res. 2014;114:1611-1622. doi: 10.1161/CIRCRESAHA.114.303204.
32. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, Locati M, Mantovani A, Martinez FO, Mege JL, Mosser DM, Natoli G, Saeij JP, Schultze JL, Shirey KA, Sica A, Suttles J, Udalova I, van Ginderachter JA, Vogel SN, Wynn TA. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41:14-20. doi: 10.1016/j. immuni.2014.06.008.
33. Stockmann C, Kerdiles Y, Nomaksteinsky M, Weidemann A, Takeda N, Doedens A, Torres-Collado AX, Iruela-Arispe L, Nizet V, Johnson RS. Loss of myeloid cell-derived vascular endothelial growth factor accelerates fibrosis. Proc Natl Acad Sci USA. 2010;107:4329-4334. doi: 10.1073/pnas.0912766107.
34. Wan E, Yeap XY, Dehn S, Terry R, Novak M, Zhang S, Iwata S, Han X, Homma S, Drosatos K, Lomasney J, Engman DM, Miller SD, Vaughan DE, Morrow JP, Kishore R, Thorp EB. Enhanced efferocytosis of apoptotic cardiomyocytes through myeloid-epithelial-reproductive tyrosine kinase links acute inflammation resolution to cardiac repair after infarction. Circ Res. 2013;113:1004-1012. doi: 10.1161/CIRCRESAHA.113.301198.
35. Wu Y, Singh S, Georgescu MM, Birge RB. A role for Mer tyrosine kinase in alphavbeta5 integrin-mediated phagocytosis of apoptotic cells. J Cell Sci. 2005;118(pt 3):539-553. doi: 10.1242/jcs.01632.
36. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG, Gordonov S, Mazloom AR, Ma'ayan A, Chua WJ, Hansen TH, Turley SJ, Merad M, Randolph GJ; Immunological Genome Consortium. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol. 2012;13:1118-1128. doi: 10.1038/ni.2419.
37. Cochain C, Channon KM, Silvestre JS. Angiogenesis in the infarcted myocardium. Antioxid Redox Signal. 2013;18:1100-1113. doi: 10.1089/ars.2012.4849.
38. Kantari-Mimoun C, Castells M, Klose R, Meinecke AK, Lemberger UJ, Rautou PE, Pinot-Roussel H, Badoual C, Schrödter K, Österreicher CH, Fandrey J, Stockmann C. Resolution of liver fibrosis requires myeloid cell-driven sinusoidal angiogenesis. Hepatology. 2015;61:2042-2055. doi: 10.1002/hep.27635.
39. Avraham-Davidi I, Yona S, Grunewald M, Landsman L, Cochain C, Silvestre JS, Mizrahi H, Faroja M, Strauss-Ayali D, Mack M, Jung S, Keshet E. On-site education of VEGF-recruited monocytes improves their performance as angiogenic and arteriogenic accessory cells. J Exp Med. 2013;210:2611-2625. doi: 10.1084/jem.20120690.
40. Torre-Amione G, Anker SD, Bourge RC, Colucci WS, Greenberg BH, Hildebrandt P, Keren A, Motro M, Moyé LA, Otterstad JE, Pratt CM, Ponikowski P, Rouleau JL, Sestier F, Winkelmann BR, Young JB; Advanced Chronic Heart Failure CLinical Assessment of Immune Modulation Therapy Investigators. Results of a non-specific immunomodulation therapy in chronic heart failure (ACCLAIM trial): a placebocontrolled randomised trial. Lancet. 2008;371:228-236. doi: 10.1016/S0140-6736(08)60134-8.
41. Harel-Adar T, Ben Mordechai T, Amsalem Y, Feinberg MS, Leor J, Cohen S. Modulation of cardiac macrophages by phosphatidylserinepresenting liposomes improves infarct repair. Proc Natl Acad Sci USA. 2011;108:1827-1832. doi: 10.1073/pnas.1015623108.